Insect Succession and Extended Time of Colonization

Arthropods associated with carrion are associated with ecological groups: necrophagous species, which feed upon the animal remains; omnivorous species, which feed upon both the animal remains and other organisms colonizing those remains; predators and parasites of the necrophagous or omnivorous species; adventive species, which use the remains as an extension of the environment; and incidental species which are associated with animal remains due to happenstance (Smith, 1986; Roberts & Marquez-Grant, 2012).

Necrophagous insects arrive on and in a corpse in a somewhat predictable sequence and are arguably the most useful for forensic entomology. This is the ecological succession of insects, and is influenced by the environment, season, and the decompositional state of the carrion. The insects arrive in blending waves, called seres, of organisms, each comprised of different species attracted to a particular state of decay (Smith, 1986; Goff, 1993).

Early research in entomology indicated that the number of seres varies according to the placement of the carrion. Megnin (1894) showed that animals exposed to the environment yielded eight distinct insect seres, while those that were buried attracted only three distinct insect seres. This difference speaks to the availability of the tissue to colonizing insects, along with the ability of those insects to reach tissue that is blocked from easy access. Different insects are attracted to different stages of generalized decomposition. While stages of decomposition are not discrete and can sometimes be difficult to characterize with precision, historically scientists have broken up decomposition of animal remains into five major stages: fresh, putrefaction, active decay, butyric fermentation, and dry decay (Haglund & Sorg, 1996). Each of these stages attracts one or more seres of insects and other arthropods in a predictable sequence.

Table 5.3 Developmental data by species, observed temperature, and author

(Continued)

Forensic Entomologyoo cn

Table 5.3 (Continued) Developmental data by species, observed temperature, and author

Note: Data recorded in mean hours (h) or days (d) of developmental time necessary to complete individual life stage at the given standard temperature. indicates no data for a particular life stage given in publication.

^a Sarcophaga haemorrhoidalis is larviporous and therefore does not have an egg stage.

Insect Succession and Extended Time of Colonization

From the moment of death, the insect fauna of an animal body begins to change. Any ectoparasites associated with the body leave relatively quickly as the body cools and the blood ceases to circulate (Mullen & Durden, 2002). Myiasis causing flies may or may not die; it is dependent upon if they are obligate parasites of living tissue, or facultative parasites that can feed on both living and dead animals. Bot flies, for example, are dependent upon a living host, and if the host dies, the bot fly dies. Cochliomyia species, on the other hand, can feed on living or dead hosts, and may just continue to feed after the animal dies (Mullen & Durden, 2002; Byrd & Castner, 2010).

Necrophagous insects, or those attracted to dead tissue, are attracted to the body within minutes of death, and are associated with the fresh stage of decay. In general, the first adults are observed on a newly dead animal within an hour after death, as long as there is adequate access to the body (Byrd & Castner, 2010). Some investigators report female flies arriving within 15 seconds of death (Catts & Haskell, 2008). Eggs and early instar maggots tend to appear with the onset of autolysis. In general, the animal will be characterized in this early sere by the presence of adult flies and fly eggs. Eggs will be found near natural bodily opening, on wounds, and sometimes in protected folds of skin or coverings. Those eggs will hatch to first instars quickly in warm environments, but there will not be a large maggot mass on the body; the tissue will still look fresh. The most common groups of insects found during this fresh stage include species from the fly families of Calliphoridae, Muscidae, and Sarcophagidae (Schoenly & Reid, 1987; Smith, 1989).

As the carrion begins to putrefy, the young maggots will move throughout the body, spreading bacteria, secreting digestive enzymes, and feeding on tissue. They move as a maggot mass, benefitting from communal heat and shared digestive secretions. Larvae first feed between muscles, then on the muscle fibers themselves as the maggots grow and the digestive juices get to work. The rate of decay increases, and the odors emitted from the body attract more blowflies, flesh flies, beetles, and mites. They are joined by parasitic wasps that lay their eggs inside maggots and later inside pupae. The most common insects associated with this putrefaction stage, however, are species in the fly families of Calliphoridae and Sarcophagidae (Smith, 1986).

Once the carrion enters active decay, there will be several generations of maggots present on the body. Some of the maggots will be large, well into the third instar. The oldest maggots will begin to disperse from the carrion to find pupation sites. These maggots will crawl under objects in the environment, or burrow into the soil to become pupae. The early seres or pioneer flies cease to be attracted to the corpse, making way for those insects that prefer later stages of decay. Predatory maggots are much more abundant at this stage and may be feeding upon other species in the maggot mass (Nelder et al., 2009). Predatory beetles lay their eggs in the corpse and their larvae then hatch to feed on the dead animal and other insects colonizing that animal. Parasitic wasps are even more common, attacking the huge maggot masses and developing pupae. Active decay attracts a new sere characterized by beetles in Dermestidae, and grease moths. As active decay moves into butyric fermentation, two additional seres are attracted: first, a sere consisting of cheese skippers, Fannia species, spesid beetles, and beetles in the family Cleridae arrives at the body. The second sere consists of dump flies, flies in the family Phoridae, beetles in the family Silphidae, and clown beetles (Smith, 1986).

As the carrion is stripped of most of its soft tissue, the remaining tissue begins to dry out (Figure 5.8). The reduction in soft food makes the body less palatable to the mouth hooks of maggots, and more suitable for the chewing mouthparts of beetles. Beetle adults and larvae feed on skin and ligaments, while certain late stage flies, such as the cheese fly, arrive to feed on whatever moist flesh remains. Predators and parasites are still prevalent at this stage, feeding on the straggling maggots or other soft bodied insects in the vicinity (Smith, 1986; Schoenly, 1992).

Once the carrion has completely dried out, the body attracts insects that can feed on hair and dried skin (Figure 5.9). This dry stage of decomposition is highly attractive to a new sere consisting of mites, followed by a sere of beetles in Dermestidiae and Tinidae, and finally a sere of primarily Ptinidae and Tenerionidae. This stage tends to last for a long while, since the business of feeding on

Figure 5.8 (a) This bovine carcass shows the typical tissue loss around the mouth from maggot feeding, (b) Insect will colonize the anal and genital area of animals and the insect feeding may leave postmortem artefacts visible for week or months after the insects have departed the remains.

Figure 5.9 This calf shows marked decomposition in the thoracic region, a much different pattern than the cow shown in Figure 5.8. This pattern of decomposition is indicative of vertebrate scavenging. Notice the near-intact tissue along the limb and head, yet the skeletonization of the ribs. The insects had access to the thoracic cavity, which does not happen in intact carcasses. The maggot feeding was therefore concentrated around the ribs and abdominal organs, resulting in the unusual decomposition pattern shown.

□«compositional stage

Calllphorldae

Muscldae

Sarcophagldae

Phorldae

Clerldae

Sllphldae

Hlsterldae

Dermestldae

Tlneldae

Butyric

Fresh Putrefaction Active decay fermentation Dry remains

Figure 5.10 General arrival of forensically important insect families by phase of decomposition. In addition to insect development, insect succession can be utilized to estimate the postmortem interval. Insect succession is the presence or absence of insect species and the sequence in which they arrive and depart. Knowledge of insect succession in a geographic location can assist the forensic entomologist with postmortem interval estimations.

dried-out tissue takes a great deal of time and digestive enzymes. The beetles will remain on the bones as long as the carrion is undisturbed and has dried tissue (Smith, 1989).

After the dried tissue has been cleaned by the beetles, moths, and mites, only the bones remain along with empty pupal casings. There is no longer any major insect activity, and any further decomposition is accomplished by bacteria and physical factors (Haglund & Sorg, 1996).

By way of comparison, a buried animal has fewer seres with lower species diversity (Payne, 1968). Fresh buried animals tend to attract flies in Calliphoridae, Muscidae, Sarcophagidae, and Phoridae. Buried animals in active decay may attract root-eating beetles, and those in dry decay are populated by rove beetles.

Since Megnin’s original experiments, there have been numerous attempts to characterize the number of seres that show up on animals of different sizes. The consensus is that these successional waves range from 8 to 10, and any attempts to discreetly define the arthropod community associated with the seres is confounded by the continual nature of decomposition. There is a broad general agreement of orders and families that show up on a decomposing body (Smith, 1986; Catts & Haskell, 2008; Byrd & Castner, 2010). There is also a general agreement of sequence, and the idea that the first sere is primarily composed of Dipteran species. Succession is affected by the location of the carrion, any covering, animal type, local insect species, time of year, and a myriad of other factors. At the family level, succession looks like Figure 5.10. Knowing the general succession of insects on a corpse in a particular area enables the entomologist to extend the time of colonization estimation even if the primary colonizers of the first sere have come and gone.